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Virulence genes of Shiga toxin-producing Escherichia coli O157:H7 strains isolated from calves and cattle

Year 2011, , 255 - 260, 01.12.2011

Yahya Kuyucuoğlu Esra Şeker Cevdet Uğuz Barış Sareyyüpoğlu Selahattin Konak

https://doi.org/10.1501/Vetfak_0000002484
Cited By: 3

Abstract

The aim of this study was to detect E. coli O157:H7 serotype in the faeces samples collected from calves and cattle farms located of Afyonkarahisar province in Turkey and to determine the stx(1) (Shiga toxin 1) and stx(2) (Shiga toxin 2) virulence genes in the strains of E.coli O157:H7 by multiplex PCR (mPCR). In this study, E. coli O157:H7 was isolated from the 3.1% (14 out 457 faeces samples) of the calves and cattle examined, in particular 2.3% of the cattle, 2.6% of non-diarrhoeic calves and 10.6% of diarrhoeic calves were positive for E. coli O157:H7. The stx(1) and stx(2) genes were detected in 6 out of 14 (42.8%) DNA samples extracted from STEC O157:H7 strains. This study demonstrated of E. coli O157:H7 serotype in cattle and calves, which represent an important reservoir for strains that a potential risk for human infections

Keywords

Calves cattle Escherichia coli O157:H7 mPCR stx(1) and stx(2) genes

References

  • Abu-Ali GS, Oulette LM, Henderson ST, Whittam TS, Manning SD (2010). Differences in adherence and virulence gene expression between two outbreak strains of enterohemorrhagic Escherichia coli O157:H7. Microbiol, 156, 408-419.
  • Aidar Ugrinovich L, Blanco J, Blanco M, Blanco JE, Leomil L, Dahbi G, Mora A, Onuma DL, Siveira WD, Pestane de Castro AF (2007). Serotypes, virulence genes, and intimin types of Shiga toxin-producing Escherichia coli (STEC) and enteropathogenic E.coli (EPEC) isolated from calves in Sao Paulo, Brazil. Int J Food Microbiol, 115, 297-306.
  • Armstrong G, Hollingsworth J, Morris JG (1996). Emerging foodborne pathogens: Escherichia coli O157:H7 as a model of entry of a new pathogen into the food supply of developed world. Epidemiol Rev, 18, 29-51.
  • Aslantas Ö, Erdogan S, Cantekin Z, Gülacti I, Evrendilek GA (2006). Isolation and characterization of verocytotoxin-producing Escherichia coli O157 from Turkish cattle. Int J Food Microbiol, 106, 338-342.
  • Baines D, Lee B, McAllister T (2008). Heterogeneity in enterohemorrhagic Escherichia coli O157:H7 fecal shedding in cattle is related to Escherichia coli O157:H7 colonization of the small and large intestine. Can J Microbiol, 54, 984-95.
  • Barret TJ, Kaper JB, Jarse AE, Wachsmuth IK (1992). Virulence factors in Shiga-like toxin-producing Escherichia coli isolated from humans and cattle. J Infect Dis, 165, 979-980.
  • Beutin L (1999). Escherichia coli O157 and Other Types of Verocytotoxigenic E.coli (VTEC) Isolated from Humans, Animals and Food in Germany. 121-145. In: Stewart, C.S., and H.J. Flint (eds), Escherichia coli O157 in Farm Animals. Wallingford, UK
  • Beutin L, Geiger D, Steinruck H, Zimmermann S, Scheutz F (1993). Prevalence and some properties of verotoxin (Shiga-like toxin)-producing Escherichia coli in seven different species of healthy domestic animals. J Clin Microbiol, 31, 2483-2488.
  • Bielaszewska M, Janda J, Blahova K, Minarikova H, Jikova E, Karmali MA, Laubova J, Sikulova J, Preston MA, Khakhria R, Karch H, Klazorova H, Nye O (1997). Human Escherichia coli O157:H7 infection associated with the consumption of unpasteurized goat’s milk. Epidemiol Infec, 119, 299-305.
  • Blanco J, Blanco M, Blanco JE, Mora A, Alonso MP, Gonzalez EA, Bernardez MI (2001). Verocytotoxigenic Escherichia coli. 113-148. In: G. Duffy, P. Garvey, and D. A. McDo- well (eds), Epidemiology of Verocytotoxigenic Escherichia coli (VTEC) in Ruminants, Food & Nutrition Press Inc., Trumbull, CT, USA.
  • Brown CA, Harmon BG, Zhao T, Doyle MP (1997). Experimental Escherichia coli O157:H7 carriage in calves. Appl Environ Microbiol, 63, 27-32.
  • Caprioli A, Morabito S, Brugere H, Oswald E (2005). Enterohaemorrhagic Escherichia coli: emerging issues on virulence and modes of transmission. Vet Res, 36, 289- 311.
  • Chapman PA, Siddons CA, Wright DJ, Norma P, Fox J, Crick E (1993). Cattle as a possible source of verocytotoxin-producing Escherichia coli O157 infections in man. Epidemiol Infect, 111, 439-447.
  • Cabalar M, Boynukara B, Gülhan T, Ekin IH (2001). Van yöresinde sağlıklı görülen süt sığırcılığı işletmelerinde Rotavirus, E. coli K99 and O157:H7’nin varlığı üzerine araştırmalar. Turk J Vet Anim Sci, 25, 191-196.
  • Dean-Nystrom EA, Bosworth BT, Cray WC, Moon HW (1997). Pathogenicity of Escherichia coli O157:H7 in the intestines of neonatal calves. Infect Immun, 65, 1842- 1848.
  • Gioffre′ A, Meichtri L, Miliwebsky E, Baschkier A, Chillemi G, Romano MI, Sosa Estani S, Cataldi A, Rodrı′guez R, Rivas M (2002). Detection of Shiga toxin- producing Escherichia coli by PCR in cattle in Argentina Evaluation of two procedures. Vet Microbiol, 87, 301-313.
  • Gyles CL (2007). Shiga toxin-producing Escherichia coli:
  • an overview. J Anim Sci, 85, 45–62.
  • Holth JG, Krieg, NR, Sneath, PHA, Staley JT, Williams ST (2000). Bergey’s manual of determinative bacteriology. Lippincott Williams & Wilkins, Philadelphia
  • Kang SJ, Ryu SJ, Chae JS, Eo SK, Woo GJ, Lee LH (2004). Occurrence and characteristics of enterohemorrhagic Escherichia coli O157 in calves associated with diarrhoea. Vet Microbiol, 98, 323-328.
  • Karnali MA, Gannon V, Sargeant JM (2009). Verocytotoxin-producing Escherichia coli (VTEC). Vet Microbiol, 140(3-4), 360-70.
  • Keen EJ, Elder RO (2002). Isolation of Shiga-toxigenic Escherichia coli O157 from hide surface and oral cavity of finished beef feedlot cattle. J Am Vet Med Assoc, 220, 756-763.
  • Keene W, Hedberg K, Herriot D, Hancock D, Mckay R, Barret T, Fleing D (1997). A prolonged outbreak of Escherichia coli O157:H7 infection caused by commercially distributed raw milk. J Infect Dis, 176, 815- 818.
  • Law D (2000). Virulence factors of Escherichia coli O157 and other Shiga toxin–producing E. coli. J Appl Microbiol, 88, 729-745.
  • Leomil L, Aidar-Ugrinovich L, Guth BEC, Irino K, Vettorato MP, Onuma DL, de Castro AFP (2003). Frequency of Shiga toxin-producing Escherichia coli (STEC) isolates among diarrheic and non-diarrheic calves in Brazil. Vet Microbiol, 97, 103-109.
  • Mainil JG, Duchesnes CJ, Whipp SC, Marques LRM, O’brien AD, Casey TA, Moon, HW (1987). Shiga-like toxin production and attaching effacing activity of Escherichia coli associated with calf diarrhea. Am J Vet. Res, 48, 743-748.
  • Masana MO, Leotta GA,Del Castillo LL, D’Astek BA, Palladino PM, Galli L, Vilacoba E, Carbonari C, Rodriguez HR, Rivas M (2010). Prevalence, characterization, and genotypic analysis of Escherichia coli O157:H7/NM from selected beef exporting abattoirs of Argentina. J Food Protect, 73, 649-656.
  • Mainil JG, Jacquemin ER. Kaeckenbeeck AE (1993). Association between the effacing (eae) gene and shiga-like toxin-encoding genes in Escherichia coli isolates from cattle. Am J Vet. Res, 54, 1064-1068.
  • Miyao Y, Kataoka T, Nomoto T, Kai A, Itoh T (1998). Prevalence of verotoxin-producing Escherichia coli harbored in the intestine of cattle in Japan. Vet Microbiol, 61, 137-143.
  • Nataro JP, Kaper JB (1998). Diarrheagenic Escherichia coli. Clin Microbiol Rev, 11, 142-201.
  • Ohya T, Ito H (1999): Experimental infection of calves with Escherichia coli O157:H7. J Vet Med Sci, 61, 1187- 1189.
  • Oporto B, Esteban JI, Aduriz G, Juste RA, Hurtado A (2008). Escherichia coli O157:H7 and non-O157 Shiga toxin-producing E.coli in healthy cattle, sheep and swine herds in Northern Spain. Zoonoses and Puplic Health, 55, 73-81.
  • Osek J (2003). Development of a multiplex PCR approach for the identification of shiga toxin-producing Escherichia coli strains and their major virulence factor genes. J Appl Microbiol, 95, 1217-1225.
  • Otawa K, Sato M, Sasaki T, Nonaka, J., Ito, K., Kuroki, T. and Nakai, Y (2004): Genetic analysis of shiga-toxigenic Escherichia coli isolates from cattle in a limited region. J Anim Sci, 75, 261-269.
  • Paton JC, Paton AW (1998). Pathogenesis and diagnosis of shiga toxin producing Escherichia coli infections. Clin Microbiol Rev, 11, 450-479.
  • Riley LW, Remis RS, Helgerson SD, McGee HB, Wells
  • JG, Davis BR, Hebert RJ, Olcott ES, Johnson LM, Hargrett NT (1983). Hemorrhagic colitis associated with a rare Escherichia coli serotype. N Engl J Med , 308, 681– 685.
  • Sandhu KS, Gyles CL (2002). Pathogenic Shiga toxin- producing Escherichia coli in the intestine of calves. Can J Vet Res, 66, 65-72.
  • Schmidt H, Beutin L, Karch H (1995). Molecular analysis of the plasmid-encoded hemolysin of Escherichia coli O157:H7 strain EDL 933. Infect Immun, 63, 1055- 1061.
  • Wells JG, Davis BR, Wachsmuth IK, Riley LW, Remis RS, Sokolow R, Morris GK (1983). Laboratory investigation of hemorrhagic colitis outbreaks associated with a rare Escherichia coli serotype. J Clin Microbiol, 18, 512-520.
  • Wells JG, Shipman L.D, Greene KD, Sowers EG, Green JH, Cameron DN, Downes FP, Martin ML, Grıffın PM, Ostroff SM, Potter ME, Tauxe RV, Wachsmuth KI (1991). Isolation of Escherichia coli serotype O157:H7 and other Shiga-like toxin-producing E.coli from dairy cattle. J Clin Microbiol, 29, 985-989.
  • Wieler LH, Vieler E, Erpenstein C, Schlapp T, Steinrück H, Bauerfeind R, Byomi A, Baljer G (1996). Shiga toxin-producing Escherichia coli strains from bovines: Association of adhesion with carriage of eae and other genes. J Clin Microbiol, 34, 2980-2984.
  • Yilmaz A, Gun H, Yilmaz H (2002). Frequency of Escherichia coli O157:H7 in Turkish cattle. J Food Protect, 10, 1637-1640.
  • Yilmaz A, Gun H, Ugur M, Turan N, Yilmaz H (2006). Detection and frequency of VT1, VT2 and eaeA genes in Escherichia coli O157 and O157:H7 strains isolated from cattle, cattle carcasses and abattoir environment in Istanbul. Int J Food Microbiol, 106, 213-217.
  • Zhao T, Doyle MP, Shere J, Garber L (1995). Prevalence of enterohemorrhagic Escherichia coli O157:H7 in a survey of dairy herds. Appl Environ Microbiol, 61, 1290-1293.

İnek ve buzağılardan izole edilen Şiga toksijenik Escherichia coli O157:H7 suşlarının bazı virülensgenleri

Year 2011, , 255 - 260, 01.12.2011

Yahya Kuyucuoğlu Esra Şeker Cevdet Uğuz Barış Sareyyüpoğlu Selahattin Konak

https://doi.org/10.1501/Vetfak_0000002484
Cited By: 3

Abstract

Bu çalışmanın amacı, Afyonkarahisar’da bulunan çifliklerdeki inek ve buzağılardan toplanan dışkı örneklerinden E. coli O157:H7 serotiplerini izole etmek, stx(1) (Şiga toksin 1) ve stx(2) (Şiga toksin 2) virülens genlerini multipleks PCR (mPCR) ile belirlemektir. Bu çalışmada, inek ve buzağılardan alınan toplam 457 dışkı örneğinin 14 (%3.1)’ünden E. coli O157:H7 serotipi izole edildi. İzole edilen suşların %2.3’ü ineklerden, %2.6’sı sağlıklı buzağılardan, %10.6’sı ise ishalli buzağılardan elde edildi. Şigatoksijenik E. coli (STEC) O157:H7 suşlarından elde edilen 14 DNA örneğinin 6 (%42.8)’sında stx(1) ve stx(2) geni pozitif bulundu. Bu çalışma, inek ve buzağılardan izole edilen STEC O157:H7 serotiplerinin insan enfeksiyonları için önemli bir risk faktörü olabileceğini göstermektedir

Keywords

Buzağı Escherichia coli O157:H7 inek mPCR stx(1) ve stx(2) genleri

References

  • Abu-Ali GS, Oulette LM, Henderson ST, Whittam TS, Manning SD (2010). Differences in adherence and virulence gene expression between two outbreak strains of enterohemorrhagic Escherichia coli O157:H7. Microbiol, 156, 408-419.
  • Aidar Ugrinovich L, Blanco J, Blanco M, Blanco JE, Leomil L, Dahbi G, Mora A, Onuma DL, Siveira WD, Pestane de Castro AF (2007). Serotypes, virulence genes, and intimin types of Shiga toxin-producing Escherichia coli (STEC) and enteropathogenic E.coli (EPEC) isolated from calves in Sao Paulo, Brazil. Int J Food Microbiol, 115, 297-306.
  • Armstrong G, Hollingsworth J, Morris JG (1996). Emerging foodborne pathogens: Escherichia coli O157:H7 as a model of entry of a new pathogen into the food supply of developed world. Epidemiol Rev, 18, 29-51.
  • Aslantas Ö, Erdogan S, Cantekin Z, Gülacti I, Evrendilek GA (2006). Isolation and characterization of verocytotoxin-producing Escherichia coli O157 from Turkish cattle. Int J Food Microbiol, 106, 338-342.
  • Baines D, Lee B, McAllister T (2008). Heterogeneity in enterohemorrhagic Escherichia coli O157:H7 fecal shedding in cattle is related to Escherichia coli O157:H7 colonization of the small and large intestine. Can J Microbiol, 54, 984-95.
  • Barret TJ, Kaper JB, Jarse AE, Wachsmuth IK (1992). Virulence factors in Shiga-like toxin-producing Escherichia coli isolated from humans and cattle. J Infect Dis, 165, 979-980.
  • Beutin L (1999). Escherichia coli O157 and Other Types of Verocytotoxigenic E.coli (VTEC) Isolated from Humans, Animals and Food in Germany. 121-145. In: Stewart, C.S., and H.J. Flint (eds), Escherichia coli O157 in Farm Animals. Wallingford, UK
  • Beutin L, Geiger D, Steinruck H, Zimmermann S, Scheutz F (1993). Prevalence and some properties of verotoxin (Shiga-like toxin)-producing Escherichia coli in seven different species of healthy domestic animals. J Clin Microbiol, 31, 2483-2488.
  • Bielaszewska M, Janda J, Blahova K, Minarikova H, Jikova E, Karmali MA, Laubova J, Sikulova J, Preston MA, Khakhria R, Karch H, Klazorova H, Nye O (1997). Human Escherichia coli O157:H7 infection associated with the consumption of unpasteurized goat’s milk. Epidemiol Infec, 119, 299-305.
  • Blanco J, Blanco M, Blanco JE, Mora A, Alonso MP, Gonzalez EA, Bernardez MI (2001). Verocytotoxigenic Escherichia coli. 113-148. In: G. Duffy, P. Garvey, and D. A. McDo- well (eds), Epidemiology of Verocytotoxigenic Escherichia coli (VTEC) in Ruminants, Food & Nutrition Press Inc., Trumbull, CT, USA.
  • Brown CA, Harmon BG, Zhao T, Doyle MP (1997). Experimental Escherichia coli O157:H7 carriage in calves. Appl Environ Microbiol, 63, 27-32.
  • Caprioli A, Morabito S, Brugere H, Oswald E (2005). Enterohaemorrhagic Escherichia coli: emerging issues on virulence and modes of transmission. Vet Res, 36, 289- 311.
  • Chapman PA, Siddons CA, Wright DJ, Norma P, Fox J, Crick E (1993). Cattle as a possible source of verocytotoxin-producing Escherichia coli O157 infections in man. Epidemiol Infect, 111, 439-447.
  • Cabalar M, Boynukara B, Gülhan T, Ekin IH (2001). Van yöresinde sağlıklı görülen süt sığırcılığı işletmelerinde Rotavirus, E. coli K99 and O157:H7’nin varlığı üzerine araştırmalar. Turk J Vet Anim Sci, 25, 191-196.
  • Dean-Nystrom EA, Bosworth BT, Cray WC, Moon HW (1997). Pathogenicity of Escherichia coli O157:H7 in the intestines of neonatal calves. Infect Immun, 65, 1842- 1848.
  • Gioffre′ A, Meichtri L, Miliwebsky E, Baschkier A, Chillemi G, Romano MI, Sosa Estani S, Cataldi A, Rodrı′guez R, Rivas M (2002). Detection of Shiga toxin- producing Escherichia coli by PCR in cattle in Argentina Evaluation of two procedures. Vet Microbiol, 87, 301-313.
  • Gyles CL (2007). Shiga toxin-producing Escherichia coli:
  • an overview. J Anim Sci, 85, 45–62.
  • Holth JG, Krieg, NR, Sneath, PHA, Staley JT, Williams ST (2000). Bergey’s manual of determinative bacteriology. Lippincott Williams & Wilkins, Philadelphia
  • Kang SJ, Ryu SJ, Chae JS, Eo SK, Woo GJ, Lee LH (2004). Occurrence and characteristics of enterohemorrhagic Escherichia coli O157 in calves associated with diarrhoea. Vet Microbiol, 98, 323-328.
  • Karnali MA, Gannon V, Sargeant JM (2009). Verocytotoxin-producing Escherichia coli (VTEC). Vet Microbiol, 140(3-4), 360-70.
  • Keen EJ, Elder RO (2002). Isolation of Shiga-toxigenic Escherichia coli O157 from hide surface and oral cavity of finished beef feedlot cattle. J Am Vet Med Assoc, 220, 756-763.
  • Keene W, Hedberg K, Herriot D, Hancock D, Mckay R, Barret T, Fleing D (1997). A prolonged outbreak of Escherichia coli O157:H7 infection caused by commercially distributed raw milk. J Infect Dis, 176, 815- 818.
  • Law D (2000). Virulence factors of Escherichia coli O157 and other Shiga toxin–producing E. coli. J Appl Microbiol, 88, 729-745.
  • Leomil L, Aidar-Ugrinovich L, Guth BEC, Irino K, Vettorato MP, Onuma DL, de Castro AFP (2003). Frequency of Shiga toxin-producing Escherichia coli (STEC) isolates among diarrheic and non-diarrheic calves in Brazil. Vet Microbiol, 97, 103-109.
  • Mainil JG, Duchesnes CJ, Whipp SC, Marques LRM, O’brien AD, Casey TA, Moon, HW (1987). Shiga-like toxin production and attaching effacing activity of Escherichia coli associated with calf diarrhea. Am J Vet. Res, 48, 743-748.
  • Masana MO, Leotta GA,Del Castillo LL, D’Astek BA, Palladino PM, Galli L, Vilacoba E, Carbonari C, Rodriguez HR, Rivas M (2010). Prevalence, characterization, and genotypic analysis of Escherichia coli O157:H7/NM from selected beef exporting abattoirs of Argentina. J Food Protect, 73, 649-656.
  • Mainil JG, Jacquemin ER. Kaeckenbeeck AE (1993). Association between the effacing (eae) gene and shiga-like toxin-encoding genes in Escherichia coli isolates from cattle. Am J Vet. Res, 54, 1064-1068.
  • Miyao Y, Kataoka T, Nomoto T, Kai A, Itoh T (1998). Prevalence of verotoxin-producing Escherichia coli harbored in the intestine of cattle in Japan. Vet Microbiol, 61, 137-143.
  • Nataro JP, Kaper JB (1998). Diarrheagenic Escherichia coli. Clin Microbiol Rev, 11, 142-201.
  • Ohya T, Ito H (1999): Experimental infection of calves with Escherichia coli O157:H7. J Vet Med Sci, 61, 1187- 1189.
  • Oporto B, Esteban JI, Aduriz G, Juste RA, Hurtado A (2008). Escherichia coli O157:H7 and non-O157 Shiga toxin-producing E.coli in healthy cattle, sheep and swine herds in Northern Spain. Zoonoses and Puplic Health, 55, 73-81.
  • Osek J (2003). Development of a multiplex PCR approach for the identification of shiga toxin-producing Escherichia coli strains and their major virulence factor genes. J Appl Microbiol, 95, 1217-1225.
  • Otawa K, Sato M, Sasaki T, Nonaka, J., Ito, K., Kuroki, T. and Nakai, Y (2004): Genetic analysis of shiga-toxigenic Escherichia coli isolates from cattle in a limited region. J Anim Sci, 75, 261-269.
  • Paton JC, Paton AW (1998). Pathogenesis and diagnosis of shiga toxin producing Escherichia coli infections. Clin Microbiol Rev, 11, 450-479.
  • Riley LW, Remis RS, Helgerson SD, McGee HB, Wells
  • JG, Davis BR, Hebert RJ, Olcott ES, Johnson LM, Hargrett NT (1983). Hemorrhagic colitis associated with a rare Escherichia coli serotype. N Engl J Med , 308, 681– 685.
  • Sandhu KS, Gyles CL (2002). Pathogenic Shiga toxin- producing Escherichia coli in the intestine of calves. Can J Vet Res, 66, 65-72.
  • Schmidt H, Beutin L, Karch H (1995). Molecular analysis of the plasmid-encoded hemolysin of Escherichia coli O157:H7 strain EDL 933. Infect Immun, 63, 1055- 1061.
  • Wells JG, Davis BR, Wachsmuth IK, Riley LW, Remis RS, Sokolow R, Morris GK (1983). Laboratory investigation of hemorrhagic colitis outbreaks associated with a rare Escherichia coli serotype. J Clin Microbiol, 18, 512-520.
  • Wells JG, Shipman L.D, Greene KD, Sowers EG, Green JH, Cameron DN, Downes FP, Martin ML, Grıffın PM, Ostroff SM, Potter ME, Tauxe RV, Wachsmuth KI (1991). Isolation of Escherichia coli serotype O157:H7 and other Shiga-like toxin-producing E.coli from dairy cattle. J Clin Microbiol, 29, 985-989.
  • Wieler LH, Vieler E, Erpenstein C, Schlapp T, Steinrück H, Bauerfeind R, Byomi A, Baljer G (1996). Shiga toxin-producing Escherichia coli strains from bovines: Association of adhesion with carriage of eae and other genes. J Clin Microbiol, 34, 2980-2984.
  • Yilmaz A, Gun H, Yilmaz H (2002). Frequency of Escherichia coli O157:H7 in Turkish cattle. J Food Protect, 10, 1637-1640.
  • Yilmaz A, Gun H, Ugur M, Turan N, Yilmaz H (2006). Detection and frequency of VT1, VT2 and eaeA genes in Escherichia coli O157 and O157:H7 strains isolated from cattle, cattle carcasses and abattoir environment in Istanbul. Int J Food Microbiol, 106, 213-217.
  • Zhao T, Doyle MP, Shere J, Garber L (1995). Prevalence of enterohemorrhagic Escherichia coli O157:H7 in a survey of dairy herds. Appl Environ Microbiol, 61, 1290-1293.
There are 45 citations in total.

Details

Primary Language English
Subjects Veterinary Surgery
Other ID JA96RR54VJ
Journal Section Research Article
Authors

Yahya Kuyucuoğlu

Esra Şeker

Cevdet Uğuz

Barış Sareyyüpoğlu

Selahattin Konak

Publication Date December 1, 2011
Published in Issue Year 2011

Cite

APA Kuyucuoğlu, Y., Şeker, E., Uğuz, C., Sareyyüpoğlu, B., et al. (2011). Virulence genes of Shiga toxin-producing Escherichia coli O157:H7 strains isolated from calves and cattle. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 58(4), 255-260. https://doi.org/10.1501/Vetfak_0000002484
AMA Kuyucuoğlu Y, Şeker E, Uğuz C, Sareyyüpoğlu B, Konak S. Virulence genes of Shiga toxin-producing Escherichia coli O157:H7 strains isolated from calves and cattle. Ankara Univ Vet Fak Derg. December 2011;58(4):255-260. doi:10.1501/Vetfak_0000002484
Chicago Kuyucuoğlu, Yahya, Esra Şeker, Cevdet Uğuz, Barış Sareyyüpoğlu, and Selahattin Konak. “Virulence Genes of Shiga Toxin-Producing Escherichia Coli O157:H7 Strains Isolated from Calves and Cattle”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 58, no. 4 (December 2011): 255-60. https://doi.org/10.1501/Vetfak_0000002484.
EndNote Kuyucuoğlu Y, Şeker E, Uğuz C, Sareyyüpoğlu B, Konak S (December 1, 2011) Virulence genes of Shiga toxin-producing Escherichia coli O157:H7 strains isolated from calves and cattle. Ankara Üniversitesi Veteriner Fakültesi Dergisi 58 4 255–260.
IEEE Y. Kuyucuoğlu, E. Şeker, C. Uğuz, B. Sareyyüpoğlu, and S. Konak, “Virulence genes of Shiga toxin-producing Escherichia coli O157:H7 strains isolated from calves and cattle”, Ankara Univ Vet Fak Derg, vol. 58, no. 4, pp. 255–260, 2011, doi: 10.1501/Vetfak_0000002484.
ISNAD Kuyucuoğlu, Yahya et al. “Virulence Genes of Shiga Toxin-Producing Escherichia Coli O157:H7 Strains Isolated from Calves and Cattle”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 58/4 (December 2011), 255-260. https://doi.org/10.1501/Vetfak_0000002484.
JAMA Kuyucuoğlu Y, Şeker E, Uğuz C, Sareyyüpoğlu B, Konak S. Virulence genes of Shiga toxin-producing Escherichia coli O157:H7 strains isolated from calves and cattle. Ankara Univ Vet Fak Derg. 2011;58:255–260.
MLA Kuyucuoğlu, Yahya et al. “Virulence Genes of Shiga Toxin-Producing Escherichia Coli O157:H7 Strains Isolated from Calves and Cattle”. Ankara Üniversitesi Veteriner Fakültesi Dergisi, vol. 58, no. 4, 2011, pp. 255-60, doi:10.1501/Vetfak_0000002484.
Vancouver Kuyucuoğlu Y, Şeker E, Uğuz C, Sareyyüpoğlu B, Konak S. Virulence genes of Shiga toxin-producing Escherichia coli O157:H7 strains isolated from calves and cattle. Ankara Univ Vet Fak Derg. 2011;58(4):255-60.

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